Neuroplasticity of imagined wrist actions after spinal cord injury: a pilot study

Experimental Brain Research

Volumn 233, Issue 1, 2015, Pages 291-302

  Di Rienzo, Franck ^a   Guillot, Aymeric ^a,e   Mateo, Sébastien ^a,b,c   Daligault, Sébastien ^c   Delpuech, Claude ^c   Rode, Gilles ^b,d   Collet, Christian ^a  

^a UNIVERSITÉ LYON 1   (France)

^b Hopital Henry Gabrielle   (France)

^c CERMEP IMAGERIE DU VIVANT   (France)

^d LYON NEUROSCIENCE RESEARCH CENTER   (France)

^e INSTITUT UNIVERSITAIRE DE FRANCE   (France)

Author keywords

Magnetoencephalography; Motor imagery; Rehabilitation; Spinal cord injury

Indexed keywords

ADULT; AMERICAN SPINAL INJURY ASSOCIATION IMPAIRMENT SCALE; ARTICLE; CONTROLLED STUDY; HUMAN; IMAGERY; MAGNETOENCEPHALOGRAPHY; MOTOR PERFORMANCE; NERVE CELL PLASTICITY; NEUROPHYSIOLOGICAL RECRUITMENT; PHYSIOTHERAPY; PILOT STUDY; PRIORITY JOURNAL; SPINAL CORD INJURY; TENODESIS; FEMALE; HAND STRENGTH; IMAGINATION; MALE; MOVEMENT (PHYSIOLOGY); PATHOPHYSIOLOGY; PHYSIOLOGY; SPINAL CORD INJURIES; TREATMENT OUTCOME; WRIST; YOUNG ADULT;

ADULT; FEMALE; HAND STRENGTH; HUMANS; IMAGINATION; MAGNETOENCEPHALOGRAPHY; MALE; MOVEMENT; NEURONAL PLASTICITY; PILOT PROJECTS; SPINAL CORD INJURIES; TREATMENT OUTCOME; WRIST; WRIST JOINT; YOUNG ADULT;

EID: 84922080216     PISSN: 00144819     EISSN: 14321106     Source Type: Journal    
DOI: 10.1007/s00221-014-4114-7     Document Type: Article

References (77)

1. Alkadhi H, Brugger P, Boendermaker SH, Crelier G, Curt A, Hepp-Reymond MC, Kollias SS (2005) What disconnection tells about motor imagery: evidence from paraplegic patients. Cereb Cortex 15(2):131–140. doi:10.1093/cercor/bhh116
2. Baguley T (2012) Serious stats: a guide to advanced statistics for the behavioral sciences. Palgrave Macmillan, Basingstoke
3. Bates D, Maechler M, Bolker B, Walker S (2014) lme4: linear mixed-effects models using Eigen and S4. R package version 1.0-6. http://CRAN.R-project.org/package=lme4
4. Burianova H, Marstaller L, Sowman P, Tesan G, Rich AN, Williams M, Savage G, Johnson BW (2013) Multimodal functional imaging of motor imagery using a novel paradigm. NeuroImage. doi:10.1016/j.neuroimage.2013.01.001
5. Chang Y, Lee JJ, Seo JH, Song HJ, Kim YT, Lee HJ, Kim HJ, Lee J, Kim W, Woo M, Kim JG (2011) Neural correlates of motor imagery for elite archers. NMR Biomed 24(4):366–372. doi:10.1002/nbm.1600
6. Cox RW (1996) AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. Comput Biomed Res 29(3):162–173
7. Cramer SC, Orr EL, Cohen MJ, Lacourse MG (2007) Effects of motor imagery training after chronic, complete spinal cord injury. Exp Brain Res 177(2):233–242. doi:10.1007/s00221-006-0662-9
8. Curt A, Van Hedel HJ, Klaus D, Dietz V (2008) Recovery from a spinal cord injury: significance of compensation, neural plasticity, and repair. J Neurotrauma 25(6):677–685. doi:10.1089/neu.2007.0468
9. Davids K, Bennett S, Newell KM (2006) Movement system variability. Human Kinetics Publishers, Champaign
10. Debarnot U, Sperduti M, Di Rienzo F, Guillot A (2014) Experts bodies, experts minds: how physical and mental training shape the brain. Front Hum Neurosci 8:280. doi:10.3389/fnhum.2014.00280
11. Di Rienzo F, Guillot A, Daligault S, Delpuech C, Rode G, Collet C (2013) Motor inhibition during motor imagery: a MEG study with a quadriplegic patient. Neurocase. doi:10.1080/13554794.2013.826685
12. Di Rienzo F, Collet C, Hoyek N, Guillot A (2014a) Impact of neurologic deficits on motor imagery: a systematic review of clinical evaluations. Neuropsychol Rev. doi:10.1007/s11065-014-9257-6
13. Di Rienzo F, Guillot A, Mateo S, Daligault S, Delpuech C, Rode G, Collet C (2014b) Neuroplasticity of prehensile neural networks after quadriplegia. Neuroscience. doi:10.1016/j.neuroscience.2014.05.021
14. Dobkin BH (1993) Neuroplasticity. Key to recovery after central nervous system injury. West J Med 159(1):56–60
15. Eckert HM (1974) Variability in skill acquisition. Child Dev 45(2):487–489
16. Grangeon M, Guillot A, Sancho PO, Picot M, Revol P, Rode G, Collet C (2010) Rehabilitation of the elbow extension with motor imagery in a patient with quadriplegia after tendon transfer. Arch Phys Med Rehabil 91(7):1143–1146. doi:10.1016/j.apmr.2010.04.011
17. Grangeon M, Revol P, Guillot A, Rode G, Collet C (2012) Could motor imagery be effective in upper limb rehabilitation of individuals with spinal cord injury? A case study. Spinal Cord 50(10):766–771. doi:10.1038/sc.2012.41
18. Green JB, Sora E, Bialy Y, Ricamato A, Thatcher RW (1998) Cortical sensorimotor reorganization after spinal cord injury: an electroencephalographic study. Neurology 50(4):1115–1121. doi:10.1212/WNL.50.4.1115
19. Green JB, Sora E, Bialy Y, Ricamato A, Thatcher RW (1999) Cortical motor reorganization after paraplegia: an EEG study. Neurology 53(4):736–743. doi:10.1212/WNL.53.4.736
20. Guillot A, Collet C, Nguyen VA, Malouin F, Richards C, Doyon J (2008) Functional neuroanatomical networks associated with expertise in motor imagery. NeuroImage 41(4):1471–1483. doi:10.1016/j.neuroimage.2008.03.042
21. Guillot A, Di Rienzo F, Macintyre T, Moran A, Collet C (2012) Imagining is not doing but involves specific motor commands: a review of experimental data related to motor inhibition. Front Hum Neurosci 6:1–22. doi:10.3389/fnhum.2012.00247
22. Hoffmann G, Laffont I, Roby-Brami A (2002) Coordination of reaching movements in patients with a cervical spinal cord injury. Cahiers de psychologie cognitive 21:305–340
23. Hoffmann G, Laffont I, Hanneton S, Roby-Brami A (2006) How to extend the elbow with a weak or paralyzed triceps: control of arm kinematics for aiming in C6–C7 quadriplegic patients. Neuroscience 139(2):749–765. doi:10.1016/j.neuroscience.2005.12.018
24. Holm S (1979) A simple sequentially rejective multiple test procedure. Scand J Stat 6:65–70. doi:10.2307/4615733
25. Hotz-Boendermaker S, Funk M, Summers P, Brugger P, Hepp-Reymond MC, Curt A, Kollias SS (2008) Preservation of motor programs in paraplegics as demonstrated by attempted and imagined foot movements. NeuroImage 39(1):383–394. doi:10.1016/j.neuroimage.2007.07.065
26. Jackson PL, Lafleur MF, Malouin F, Richards CL, Doyon J (2003) Functional cerebral reorganization following motor sequence learning through mental practice with motor imagery. NeuroImage 20(2):1171–1180. doi:10.1016/s1053-8119(03)00369-0
27. Jeannerod M (1994) The representing brain: neural correlates of motor intention and imagery. Behav Brain Sci 17(02):187–202. doi:10.1017/S0140525X00034026
28. Jeannerod M (2001) Neural simulation of action: a unifying mechanism for motor cognition. NeuroImage 14(1 Pt 2):S103–S109. doi:10.1006/nimg.2001.0832
29. Jeannerod M, Frak V (1999) Mental imaging of motor activity in humans. Curr Opin Neurobiol 9(6):735–739
30. Jurkiewicz MT, Mikulis DJ, McIlroy WE, Fehlings MG, Verrier MC (2007) Sensorimotor cortical plasticity during recovery following spinal cord injury: a longitudinal fMRI study. Neurorehabil Neural Repair 21(6):527–538. doi:10.1177/1545968307301872
31. Kakulas BA (2004) Neuropathology: the foundation for new treatments in spinal cord injury. Spinal Cord 42(10):549–563. doi:10.1038/sj.sc.3101670
32. Kokotilo KJ, Eng JJ, Curt A (2009) Reorganization and preservation of motor control of the brain in spinal cord injury: a systematic review. J Neurotrauma 26(11):2113–2126. doi:10.1089/neu.2008.0688
33. Lacourse MG, Turner JA, Randolph-Orr E, Schandler SL, Cohen MJ (2004) Cerebral and cerebellar sensorimotor plasticity following motor imagery-based mental practice of a sequential movement. J Rehabil Res Dev 41(4):505–524
34. Laffont I, Briand E, Dizien O, Combeaud M, Bussel B, Revol M, Roby-Brami A (2000) Kinematics of prehension and pointing movements in C6 quadriplegic patients. Spinal Cord 38(6):354–362
35. Levy WJ Jr, Amassian VE, Traad M, Cadwell J (1990) Focal magnetic coil stimulation reveals motor cortical system reorganized in humans after traumatic quadriplegia. Brain Res 510(1):130–134. doi:10.1016/0006-8993(90)90738-w
36. Lopes da Silva FH (2010) Electrophysiological basis of MEG signals. In: Hansen PC, Kringelbach ML, Salmelin R (eds) MEG. An introduction to methods. Oxford university press, New York, pp 1–23
37. Lotze M, Halsband U (2006) Motor imagery. J Physiol Paris 99(4–6):386–395. doi:10.1016/j.jphysparis.2006.03.012
38. Lotze M, Montoya P, Erb M, Hulsmann E, Flor H, Klose U, Birbaumer N, Grodd W (1999) Activation of cortical and cerebellar motor areas during executed and imagined hand movements: an fMRI study. J Cogn Neurosci 11(5):491–501. doi:10.1162/089892999563553
39. Louis M, Guillot A, Maton S, Doyon J, Collet C (2008) Effect of imagined movement speed on subsequent motor performance. J Mot Behav 40(2):117–132. doi:10.3200/JMBR.40.2.117-132
40. Malouin F, Richards CL (2010) Mental practice for relearning locomotor skills. Phys Ther 90(2):240–251. doi:10.2522/ptj.20090029
41. Malouin F, Richards CL, Jackson PL, Lafleur MF, Durand A, Doyon J (2007) The Kinesthetic and Visual Imagery Questionnaire (KVIQ) for assessing motor imagery in persons with physical disabilities: a reliability and construct validity study. J Neurol Phys Ther 31(1):20–29. doi:10.1097/01.NPT.0000260567.24122.64
42. Malouin F, Jackson PL, Richards CL (2013) Towards the integration of mental practice in rehabilitation programs. A critical review. Front Hum Neurosci. doi:10.3389/fnhum.2013.00576
43. Mateo S, Revol P, Fourtassi M, Rossetti Y, Collet C, Rode G (2013) Kinematic characteristics of tenodesis grasp in C6 quadriplegia. Spinal Cord 51(2):144–149. doi:10.1038/sc.2012.101
44. Maynard FM Jr, Bracken MB, Creasey G, Ditunno JF Jr, Donovan WH, Ducker TB, Garber SL, Marino RJ, Stover SL, Tator CH, Waters RL, Wilberger JE, Young W (1997) International standards for neurological and functional classification of spinal cord injury. American Spinal Injury Association. Spinal Cord 35(5):266–274. doi:10.1038/sj.sc.3100432
45. Milton J, Solodkin A, Hlustik P, Small SL (2007) The mind of expert motor performance is cool and focused. NeuroImage 35(2):804–813. doi:10.1016/j.neuroimage.2007.01.003
46. Müller H, Sternad D (2004) Decomposition of variability in the execution of goal-oriented tasks: three components of skill improvement. J Exp Psychol Hum Percept Perform 30(1):212–233. doi:10.1037/0096-1523.30.1.212
47. Munzert J, Lorey B, Zentgraf K (2009) Cognitive motor processes: the role of motor imagery in the study of motor representations. Brain Res Rev 60(2):306–326. doi:10.1016/j.brainresrev.2008.12.024
48. Nardone R, Holler Y, Brigo F, Seidl M, Christova M, Bergmann J, Golaszewski S, Trinka E (2013) Functional brain reorganization after spinal cord injury: systematic review of animal and human studies. Brain Res 1504:58–73. doi:10.1016/j.brainres.2012.12.034
49. Neuper C, Pfurtscheller G (2010) Electroencephalographic characteristics during motor imagery. In: Guillot A, Collet C (eds) The neurophysiological foundations of mental and motor imagery. Oxford University Press, New York, pp 65–81
50. Page SJ, Szaflarski JP, Eliassen JC, Pan H, Cramer SC (2009) Cortical plasticity following motor skill learning during mental practice in stroke. Neurorehabil Neural Repair 23(4):382–388. doi:10.1177/1545968308326427
51. Pascual-Leone A, Nguyet D, Cohen LG, Brasil-Neto JP, Cammarota A, Hallett M (1995) Modulation of muscle responses evoked by transcranial magnetic stimulation during the acquisition of new fine motor skills. J Neurophysiol 74(3):1037–1045
52. Pfurtscheller G (2000) Spatiotemporal ERD/ERS patterns during voluntary movement and motor imagery. Suppl Clin Neurophysiol 53:196–198
53. Pfurtscheller G (2001) Functional brain imaging based on ERD/ERS. Vision Res 41(10–11):1257–1260. doi:10.1016/S0042-6989(00)00235-2
54. Pfurtscheller G, Lopes da Silva FH (1999) Event-related EEG/MEG synchronization and desynchronization: basic principles. Clin Neurophysiol 110(11):1842–1857. doi:10.1016/s1388-2457(99)00141-8
55. Pfurtscheller G, Neuper C, Brunner C, da Silva FL (2005) Beta rebound after different types of motor imagery in man. Neurosci Lett 378(3):156–159. doi:10.1016/j.neulet.2004.12.034
56. Porro CA, Francescato MP, Cettolo V, Diamond ME, Baraldi P, Zuiani C, Bazzocchi M, di Prampero PE (1996) Primary motor and sensory cortex activation during motor performance and motor imagery: a functional magnetic resonance imaging study. J Neurosci 16(23):7688–7698
57. R Core Team (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
58. Ranganathan VK, Siemionow V, Liu JZ, Sahgal V, Yue GH (2004) From mental power to muscle power–gaining strength by using the mind. Neuropsychologia 42(7):944–956. doi:10.1016/j.neuropsychologia.2003.11.018
59. Rickham PP (1964) Human experimentation. Code of Ethics of the World Medical Association. Declaration of Helsinki. Br Med J 2(5402):177
60. Robinson SE (2004) Localization of event-related activity by SAM(erf). Neurol Clin Neurophysiol 2004:109
61. Ross JS, Tkach J, Ruggieri PM, Lieber M, Lapresto E (2003) The mind’s eye: functional MR imaging evaluation of golf motor imagery. AJNR Am J Neuroradiol 24(6):1036–1044
62. Sabbah P, de Schonen S, Leveque C, Gay S, Pfefer F, Nioche C, Sarrazin JL, Barouti H, Tadie M, Cordoliani YS (2002) Sensorimotor cortical activity in patients with complete spinal cord injury: a functional magnetic resonance imaging study. J Neurotrauma 19(1):53–60. doi:10.1089/089771502753460231
63. Schlesinger I, Benyakov O, Erikh I, Suraiya S, Schiller Y (2009) Parkinson’s disease tremor is diminished with relaxation guided imagery. Mov Disord 24(14):2059–2062. doi:10.1002/mds.22671
64. Schmidt RA, Lee T (1988) Motor control and learning, 5th edn. Human Kinetics. Champaign, IL. ISBN:1450412297
65. Schmidt RA, Wrisberg CA (2004) Motor learning and performance, 3rd edn. Human Kinetics. Champaign, IL. ISBN:0-7360-6964-X
66. Schuster C, Hilfiker R, Amft O, Scheidhauer A, Andrews B, Butler J, Kischka U, Ettlin T (2011) Best practice for motor imagery: a systematic literature review on motor imagery training elements in five different disciplines. BMC Med 9:75. doi:10.1186/1741-7015-9-75
67. Snoek GJ, IJzerman MJ, Hermens HJ, Maxwell D, Biering-Sorensen F (2004) Survey of the needs of patients with spinal cord injury: impact and priority for improvement in hand function in tetraplegics. Spinal Cord 42(9):526–532. doi:10.1038/sj.sc.3101638
68. Subramanian L, Hindle JV, Johnston S, Roberts MV, Husain M, Goebel R, Linden D (2011) Real-time functional magnetic resonance imaging neurofeedback for treatment of Parkinson’s disease. J Neurosci 31(45):16309–16317. doi:10.1523/jneurosci.3498-11.2011
69. Sun L, Yin D, Zhu Y, Fan M, Zang L, Wu Y, Jia J, Bai Y, Zhu B, Hu Y (2013) Cortical reorganization after motor imagery training in chronic stroke patients with severe motor impairment: a longitudinal fMRI study. Neuroradiology. doi:10.1007/s00234-013-1188-z
70. Tadel F, Baillet S, Mosher JC, Pantazis D, Leahy RM (2011) Brainstorm: a user-friendly application for MEG/EEG analysis. Comput Intell Neurosci 2011:879716. doi:10.1155/2011/879716
71. Talairach J, Tournoux P (1988) Co-planar stereotaxic atlas of the human brain: 3-dimensional proportional System—an approach to cerebral imaging. Thieme Medical Publishers, New York
72. Tamir R, Dickstein R, Huberman M (2007) Integration of motor imagery and physical practice in group treatment applied to subjects with Parkinson’s disease. Neurorehabil Neural Repair 21(1):68–75. doi:10.1177/1545968306292608
73. Topka H, Cohen LG, Cole RA, Hallett M (1991) Reorganization of corticospinal pathways following spinal cord injury. Neurology 41(8):1276–1283. doi:10.1212/WNL.41.8.1276
74. Waters RL, Adkins RH, Yakura JS, Sie I (1993) Motor and sensory recovery following complete tetraplegia. Arch Phys Med Rehabil 74(3):242–247
75. Winter B (2013) Linear models and linear mixed effects models in R with linguistic applications. arXiv:1308.5499
76. Wirth B, Van Hedel HJ, Curt A (2008) Changes in corticospinal function and ankle motor control during recovery from incomplete spinal cord injury. J Neurotrauma 25(5):467–478. doi:10.1089/neu.2007.0472
77. Yakura JS (1996) Recovery following spinal cord injury. American Rehabilitation. http://www.thefreelibrary.com/Recovery+following+spinal+cord+injury.-a019662789